Ocean acidification stunts molluscan growth at CO2 seeps.

Ocean acidification can severely affect bivalve molluscs, especially their shell calcification. Assessing the fate of this vulnerable group in a rapidly acidifying ocean is therefore a pressing challenge. Volcanic CO2 seeps are natural analogues of future ocean conditions that offer unique insights into the scope of marine bivalves to cope with acidification. Here, we used a 2-month reciprocal transplantation of the coastal mussel Septifer bilocularis collected from reference and elevated pCO2 habitats to explore how they calcify and grow at CO2 seeps on the Pacific coast of Japan. We found significant decreases in condition index (an indication of tissue energy reserves) and shell growth of mussels living under elevated pCO2 conditions. These negative responses in their physiological performance under acidified conditions were closely associated with changes in their food sources (shown by changes to the soft tissue δ13C and δ15N ratios) and changes in their calcifying fluid carbonate chemistry (based on shell carbonate isotopic and elemental signatures). The reduced shell growth rate during the transplantation experiment was further supported by shell δ13C records along their incremental growth layers, as well as their smaller shell size despite being of comparable ontogenetic ages (5-7 years old, based on shell δ18O records). Taken together, these findings demonstrate how ocean acidification at CO2 seeps affects mussel growth and reveal that lowered shell growth helps them survive stressful conditions.

Ocean acidification increases the impact of typhoons on algal communities.

Long-term environmental change, sudden pulses of extreme perturbation, or a combination of both can trigger regime shifts by changing the processes and feedbacks which determine community assembly, structure, and function, altering the state of ecosystems. Our understanding of the mechanisms that stabilise against regime shifts or lock communities into altered states is limited, yet also critical to anticipating future states, preventing regime shifts, and reversing unwanted state change. Ocean acidification contributes to the restructuring and simplification of algal systems, however the mechanisms through which this occurs and whether additional drivers are involved requires further study. Using monthly surveys over three years at a shallow-water volcanic seep we examined how the composition of algal communities change seasonally and following periods of significant physical disturbance by typhoons at three levels of ocean acidification (equivalent to means of contemporary ∼350 and future ∼500 and 900 µatm pCO2). Sites exposed to acidification were increasingly monopolised by structurally simple, fast-growing turf algae, and were clearly different to structurally complex macrophyte-dominated reference sites. The distinct contemporary and acidified community states were stabilised and maintained at their respective sites by different mechanisms following seasonal typhoon disturbance. Macroalgal-dominated sites were resistant to typhoon damage. In contrast, significant losses of algal biomass represented a near total ecosystem reset by typhoons for the turf-dominated communities at the elevated pCO2 sites (i.e. negligible resistance). A combination of disturbance and subsequent turf recovery maintained the same simplified state between years (elevated CO2 levels promote turf growth following algal removal, inhibiting macroalgal recruitment). Thus, ocean acidification may promote shifts in algal systems towards degraded ecosystem states, and short-term disturbances which reset successional trajectories may 'lock-in' these alternative states of low structural and functional diversity.

Whole community and functional gene changes of biofilms on marine plastic debris in response to ocean acidification.

Plastics are accumulating in the world's oceans, while ocean waters are becoming acidified by increased CO2. We compared metagenome of biofilms on tethered plastic bottles in subtidal waters off Japan naturally enriched in CO2, compared to normal ambient CO2 levels. Extending from an earlier amplicon study of bacteria, we used metagenomics to provide direct insights into changes in the full range of functional genes and the entire taxonomic tree of life in the context of the changing plastisphere. We found changes in the taxonomic community composition of all branches of life. This included a large increase in diatom relative abundance across the treatments but a decrease in diatom diversity. Network complexity among families decreased with acidification, showing overall simplification of biofilm integration. With acidification, there was decreased prevalence of genes associated with cell-cell interactions and antibiotic resistance, decreased detoxification genes, and increased stress tolerance genes. There were few nutrient cycling gene changes, suggesting that the role of plastisphere biofilms in nutrient processes within an acidified ocean may not change greatly. Our results suggest that as ocean CO2 increases, the plastisphere will undergo broad-ranging changes in both functional and taxonomic composition, especially the ecologically important diatom group, with possible wider implications for ocean ecology.

Recurrent disease outbreak in a warm temperate marginal coral community.

Coral diseases contribute to the rapid degradation of coral reefs on a global scale. Although widespread in tropical and subtropical reefs, disease outbreaks have not been described in warm temperate areas. Here, we report the outbreak of a new coral disease in a warm temperate marginal coral community in Japan. Outbreaks of the disease have been observed during the summer and autumn months since 2014. It affects the coral species Porites heronensis and was tentatively named "White Mat Syndrome" (WMS) as it consists of a white microbial mat dominated by Thiothrix sp., a sulfide oxidizing bacteria. Outbreaks followed high seasonal temperatures and were associated with the macroalga Gelidium elegans, which acts as a pathogen reservoir. With ocean warming and the anticipated increase in novel coral-algae interactions as some coral species shift poleward, WMS and emerging diseases could hinder the role of temperate areas as a future coral refuge.

Decreased Diversity and Abundance of Marine Invertebrates at CO2 Seeps in Warm-Temperate Japan.

Japan has many coastal carbon dioxide seeps as it is one of the most volcanically active parts of the world. These shallow seeps do not have the spectacular aggregations of specialist fauna seen in deep-sea vent systems but they do have gradients in seawater carbonate chemistry that are useful as natural analogues of the effects of ocean acidification on marine biodiversity, ecosystem function and fisheries. Here, we compare macroinvertebrate diversity and abundance on rocky habitats at ambient (mean ≤ 410 µatm) and high (mean 971-1484 µatm) levels of seawater pCO2 in the warm-temperate region of Japan, avoiding areas with toxic sulphur or warm-water conditions. We show that although 70% of intertidal taxa and 40% of shallow subtidal taxa were able to tolerate the high CO2 conditions, there was a marked reduction in the abundance of corals, bivalves and gastropods in acidified conditions. A narrower range of filter feeders, grazers, detritivores, scavengers and carnivores were present at high CO2 resulting in a simplified coastal system that was unable to retain the high standing stocks of marine carbon biomass found in ambient conditions. It is clear that cuts in CO2 emissions would reduce the risks of climate change and ocean acidification impacts on marine biodiversity, shellfish production and biomass in the rocky coastal shores of this region.

Understanding coralline algal responses to ocean acidification: Meta-analysis and synthesis.

Ocean acidification (OA) is a major threat to the persistence of biogenic reefs throughout the world's ocean. Coralline algae are comprised of high magnesium calcite and have long been considered one of the most susceptible taxa to the negative impacts of OA. We summarize these impacts and explore the causes of variability in coralline algal responses using a review/qualitative assessment of all relevant literature, meta-analysis, quantitative assessment of critical responses, and a discussion of physiological mechanisms and directions for future research. We find that most coralline algae experienced reduced abundance, calcification rates, recruitment rates, and declines in pH within the site of calcification in laboratory experiments simulating OA or at naturally elevated CO2 sites. There were no other consistent physiological responses of coralline algae to simulated OA (e.g., photo-physiology, mineralogy, and survival). Calcification/growth was the most frequently measured parameters in coralline algal OA research, and our meta-analyses revealed greater declines in seawater pH were associated with significant decreases in calcification in adults and similar but nonsignificant trends for juveniles. Adults from the family Mesophyllumaceae also tended to be more robust to OA, though there was insufficient data to test similar trends for juveniles. OA was the dominant driver in the majority of laboratory experiments where other local or global drivers were assessed. The interaction between OA and any other single driver was often additive, though factors that changed pH at the surface of coralline algae (light, water motion, epiphytes) acted antagonistically or synergistically with OA more than any other drivers. With advances in experimental design and methodological techniques, we now understand that the physiology of coralline algal calcification largely dictates their responses to OA. However, significant challenges still remain, including improving the geographic and life-history spread of research effort and a need for holistic assessments of physiology.

Predicting responses to marine heatwaves using functional traits.

Marine heatwaves (MHWs), discrete but prolonged periods of anomalously warm seawater, can fundamentally restructure marine communities and ecosystems. Although our understanding of these events has improved in recent years, key knowledge gaps hinder our ability to predict how MHWs will affect patterns of biodiversity. Here, we outline a functional trait approach that enables a better understanding of which species and communities will be most vulnerable to MHWs, and how the distribution of species and composition of communities are likely to shift through time. Our perspective allows progress toward unifying extreme events and longer term environmental trends as co-drivers of ecological change, with the incorporation of species traits into our predictions allowing for a greater capacity to make management decisions.

Simplification, not "tropicalization", of temperate marine ecosystems under ocean warming and acidification.

Ocean warming is altering the biogeographical distribution of marine organisms. In the tropics, rising sea surface temperatures are restructuring coral reef communities with sensitive species being lost. At the biogeographical divide between temperate and tropical communities, warming is causing macroalgal forest loss and the spread of tropical corals, fishes and other species, termed "tropicalization". A lack of field research into the combined effects of warming and ocean acidification means there is a gap in our ability to understand and plan for changes in coastal ecosystems. Here, we focus on the tropicalization trajectory of temperate marine ecosystems becoming coral-dominated systems. We conducted field surveys and in situ transplants at natural analogues for present and future conditions under (i) ocean warming and (ii) both ocean warming and acidification at a transition zone between kelp and coral-dominated ecosystems. We show that increased herbivory by warm-water fishes exacerbates kelp forest loss and that ocean acidification negates any benefits of warming for range extending tropical corals growth and physiology at temperate latitudes. Our data show that, as the combined effects of ocean acidification and warming ratchet up, marine coastal ecosystems lose kelp forests but do not gain scleractinian corals. Ocean acidification plus warming leads to overall habitat loss and a shift to simple turf-dominated ecosystems, rather than the complex coral-dominated tropicalized systems often seen with warming alone. Simplification of marine habitats by increased CO2 levels cascades through the ecosystem and could have severe consequences for the provision of goods and services.

Major loss of coralline algal diversity in response to ocean acidification.

Calcified coralline algae are ecologically important in rocky habitats in the marine photic zone worldwide and there is growing concern that ocean acidification will severely impact them. Laboratory studies of these algae in simulated ocean acidification conditions have revealed wide variability in growth, photosynthesis and calcification responses, making it difficult to assess their future biodiversity, abundance and contribution to ecosystem function. Here, we apply molecular systematic tools to assess the impact of natural gradients in seawater carbonate chemistry on the biodiversity of coralline algae in the Mediterranean and the NW Pacific, link this to their evolutionary history and evaluate their potential future biodiversity and abundance. We found a decrease in the taxonomic diversity of coralline algae with increasing acidification with more than half of the species lost in high pCO2 conditions. Sporolithales is the oldest order (Lower Cretaceous) and diversified when ocean chemistry favoured low Mg calcite deposition; it is less diverse today and was the most sensitive to ocean acidification. Corallinales were also reduced in cover and diversity but several species survived at high pCO2 ; it is the most recent order of coralline algae and originated when ocean chemistry favoured aragonite and high Mg calcite deposition. The sharp decline in cover and thickness of coralline algal carbonate deposits at high pCO2 highlighted their lower fitness in response to ocean acidification. Reductions in CO2 emissions are needed to limit the risk of losing coralline algal diversity.

Feedback mechanisms stabilise degraded turf algal systems at a CO2 seep site.

Human activities are rapidly changing the structure and function of coastal marine ecosystems. Large-scale replacement of kelp forests and coral reefs with turf algal mats is resulting in homogenous habitats that have less ecological and human value. Ocean acidification has strong potential to substantially favour turf algae growth, which led us to examine the mechanisms that stabilise turf algal states. Here we show that ocean acidification promotes turf algae over corals and macroalgae, mediating new habitat conditions that create stabilising feedback loops (altered physicochemical environment and microbial community, and an inhibition of recruitment) capable of locking turf systems in place. Such feedbacks help explain why degraded coastal habitats persist after being initially pushed past the tipping point by global and local anthropogenic stressors. An understanding of the mechanisms that stabilise degraded coastal habitats can be incorporated into adaptive management to better protect the contribution of coastal systems to human wellbeing.

Ocean acidification locks algal communities in a species-poor early successional stage.

Long-term exposure to CO2 -enriched waters can considerably alter marine biological community development, often resulting in simplified systems dominated by turf algae that possess reduced biodiversity and low ecological complexity. Current understanding of the underlying processes by which ocean acidification alters biological community development and stability remains limited, making the management of such shifts problematic. Here, we deployed recruitment tiles in reference (pHT 8.137 ± 0.056 SD) and CO2 -enriched conditions (pHT 7.788 ± 0.105 SD) at a volcanic CO2 seep in Japan to assess the underlying processes and patterns of algal community development. We assessed (i) algal community succession in two different seasons (Cooler months: January-July, and warmer months: July-January), (ii) the effects of initial community composition on subsequent community succession (by reciprocally transplanting preestablished communities for a further 6 months), and (iii) the community production of resulting communities, to assess how their functioning was altered (following 12 months recruitment). Settlement tiles became dominated by turf algae under CO2 -enrichment and had lower biomass, diversity and complexity, a pattern consistent across seasons. This locked the community in a species-poor early successional stage. In terms of community functioning, the elevated pCO2 community had greater net community production, but this did not result in increased algal community cover, biomass, biodiversity or structural complexity. Taken together, this shows that both new and established communities become simplified by rising CO2 levels. Our transplant of preestablished communities from enriched CO2 to reference conditions demonstrated their high resilience, since they became indistinguishable from communities maintained entirely in reference conditions. This shows that meaningful reductions in pCO2 can enable the recovery of algal communities. By understanding the ecological processes responsible for driving shifts in community composition, we can better assess how communities are likely to be altered by ocean acidification.

Ocean acidification alters bacterial communities on marine plastic debris.

The increasing quantity of plastic waste in the ocean is providing a growing and more widespread novel habitat for microbes. Plastics have taxonomically distinct microbial communities (termed the 'Plastisphere') and can raft these unique communities over great distances. In order to understand the Plastisphere properly it will be important to work out how major ocean changes (such as warming, acidification and deoxygenation) are shaping microbial communities on waste plastics in marine environments. Here, we show that common plastic drinking bottles rapidly become colonised by novel biofilm-forming bacterial communities, and that ocean acidification greatly influences the composition of plastic biofilm assemblages. We highlight the potential implications of this community shift in a coastal community exposed to enriched CO2 conditions.

Changes in fish communities due to benthic habitat shifts under ocean acidification conditions.

Ocean acidification will likely change the structure and function of coastal marine ecosystems over coming decades. Volcanic carbon dioxide seeps generate dissolved CO2 and pH gradients that provide realistic insights into the direction and magnitude of these changes. Here, we used fish and benthic community surveys to assess the spatio-temporal dynamics of fish community properties off CO2 seeps in Japan. Adding to previous evidence from ocean acidification ecosystem studies conducted elsewhere, our findings documented shifts from calcified to non-calcified habitats with reduced benthic complexity. In addition, we found that such habitat transition led to decreased diversity of associated fish and to selection of those fish species better adapted to simplified ecosystems dominated by algae. Our data suggest that near-future projected ocean acidification levels will oppose the ongoing range expansion of coral reef-associated fish due to global warming.

Responses of Intertidal Bacterial Biofilm Communities to Increasing pCO2.

The effects of ocean acidification on ecosystems remain poorly understood, because it is difficult to simulate the effects of elevated CO2 on entire marine communities. Natural systems enriched in CO2 are being used to help understand the long-term effects of ocean acidification in situ. Here, we compared biofilm bacterial communities on intertidal cobbles/boulders and bedrock along a seawater CO2 gradient off Japan. Samples sequenced for 16S rRNA showed differences in bacterial communities with different pCO2 and between habitat types. In both habitats, bacterial diversity increased in the acidified conditions. Differences in pCO2 were associated with differences in the relative abundance of the dominant phyla. However, despite the differences in community composition, there was no indication that these changes would be significant for nutrient cycling and ecosystem function. As well as direct effects of seawater chemistry on the biofilm, increased microalgal growth and decreased grazing may contribute to the shift in bacterial composition at high CO2, as documented by other studies. Thus, the effects of changes in bacterial community composition due to globally increasing pCO2 levels require further investigation to assess the implications for marine ecosystem function. However, the apparent lack of functional shifts in biofilms along the pCO2 gradient is a reassuring indicator of stability of their ecosystem functions in shallow ocean margins.

Ocean acidification impacts on coastal ecosystem services due to habitat degradation.

The oceanic uptake of anthropogenic carbon dioxide emissions is changing seawater chemistry in a process known as ocean acidification. The chemistry of this rapid change in surface waters is well understood and readily detectable in oceanic observations, yet there is uncertainty about the effects of ocean acidification on society since it is difficult to scale-up from laboratory and mesocosm tests. Here, we provide a synthesis of the likely effects of ocean acidification on ecosystem properties, functions and services based on observations along natural gradients in pCO2. Studies at CO2 seeps worldwide show that biogenic habitats are particularly sensitive to ocean acidification and that their degradation results in less coastal protection and less habitat provisioning for fisheries. The risks to marine goods and services amplify with increasing acidification causing shifts to macroalgal dominance, habitat degradation and a loss of biodiversity at seep sites in the tropics, the sub-tropics and on temperate coasts. Based on this empirical evidence, we expect ocean acidification to have serious consequences for the millions of people who are dependent on coastal protection, fisheries and aquaculture. If humanity is able to make cuts in fossil fuel emissions, this will reduce costs to society and avoid the changes in coastal ecosystems seen in areas with projected pCO2 levels. A binding international agreement for the oceans should build on the United Nations Sustainable Development Goal to 'minimise and address the impacts of ocean acidification'.

Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical-temperate transition zone.

Rising atmospheric concentrations of carbon dioxide are causing surface seawater pH and carbonate ion concentrations to fall in a process known as ocean acidification. To assess the likely ecological effects of ocean acidification we compared intertidal and subtidal marine communities at increasing levels of pCO2 at recently discovered volcanic seeps off the Pacific coast of Japan (34° N). This study region is of particular interest for ocean acidification research as it has naturally low levels of surface seawater pCO2 (280-320 µatm) and is located at a transition zone between temperate and sub-tropical communities. We provide the first assessment of ocean acidification effects at a biogeographic boundary. Marine communities exposed to mean levels of pCO2 predicted by 2050 experienced periods of low aragonite saturation and high dissolved inorganic carbon. These two factors combined to cause marked community shifts and a major decline in biodiversity, including the loss of key habitat-forming species, with even more extreme community changes expected by 2100. Our results provide empirical evidence that near-future levels of pCO2 shift sub-tropical ecosystems from carbonate to fleshy algal dominated systems, accompanied by biodiversity loss and major simplification of the ecosystem.

Individual and population-level responses to ocean acidification.

Ocean acidification is predicted to have detrimental effects on many marine organisms and ecological processes. Despite growing evidence for direct impacts on specific species, few studies have simultaneously considered the effects of ocean acidification on individuals (e.g. consequences for energy budgets and resource partitioning) and population level demographic processes. Here we show that ocean acidification increases energetic demands on gastropods resulting in altered energy allocation, i.e. reduced shell size but increased body mass. When scaled up to the population level, long-term exposure to ocean acidification altered population demography, with evidence of a reduction in the proportion of females in the population and genetic signatures of increased variance in reproductive success among individuals. Such increased variance enhances levels of short-term genetic drift which is predicted to inhibit adaptation. Our study indicates that even against a background of high gene flow, ocean acidification is driving individual- and population-level changes that will impact eco-evolutionary trajectories.

Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming.

Ocean acidification and warming are considered two of the greatest threats to marine biodiversity, yet the combined effect of these stressors on marine organisms remains largely unclear. Using a meta-analytical approach, we assessed the biological responses of marine organisms to the effects of ocean acidification and warming in isolation and combination. As expected biological responses varied across taxonomic groups, life-history stages, and trophic levels, but importantly, combining stressors generally exhibited a stronger biological (either positive or negative) effect. Using a subset of orthogonal studies, we show that four of five of the biological responses measured (calcification, photosynthesis, reproduction, and survival, but not growth) interacted synergistically when warming and acidification were combined. The observed synergisms between interacting stressors suggest that care must be made in making inferences from single-stressor studies. Our findings clearly have implications for the development of adaptive management strategies particularly given that the frequency of stressors interacting in marine systems will be likely to intensify in the future. There is now an urgent need to move toward more robust, holistic, and ecologically realistic climate change experiments that incorporate interactions. Without them accurate predictions about the likely deleterious impacts to marine biodiversity and ecosystem functioning over the next century will not be possible.